Natural variation in root exudate composition in the genetically structured Arabidopsis thaliana in the Iberian Peninsula

Plant root exudates are involved in nutrient acquisition, microbial
partnerships, and inter-organism signaling. Yet, little is known about the
genetic and environmental drivers of root exudate variation at large
geographical scales, which may help understand evolutionary trajectories
of plants in heterogeneous environments. We quantified natural variation
in chemical composition of Arabidopsis thaliana root exudates in 105
Iberian accessions. We identified up to 373 putative compounds using
ultra-high performance liquid chromatography coupled with mass
spectrometry. We estimated broad-sense heritability of compounds and
conducted a genome-wide association (GWA) study. We associated variation
in root exudates to variation in geographic, environmental, life history,
and genetic attributes of Iberian accessions. Only 25 of 373 compounds
exhibited broad-sense heritability values significantly different from
zero. GWA analysis identified polymorphisms associated to 12 root exudate
compounds and 26 known genes involved in metabolism, defense, signaling,
and nutrient transport. The genetic structure influenced root exudate
composition involving terpenoids. We detected five terpenoids related to
plant defense significantly varying in mean abundances in two genetic
clusters. Our study provides first insights into the extent of root
exudate natural variation at a regional scale depicting a diversified
evolutionary trajectory among A. thaliana genetic clusters chiefly
mediated by terpenoid composition.